Bacterial communities associated with the Southern Ocean vent gastropod, Gigantopelta chessoia: indication of horizontal symbiont transfer
- 240 Downloads
Recently discovered hydrothermal vents of the East Scotia Ridge (ESR) in the Southern Ocean host unique faunal communities that depend on microbial chemosynthetic primary production. These highly abundant invertebrates gain energy from either grazing on free-living microbes or via hosting symbiotic chemoautotrophic microorganisms. The main objective of this study was to characterise microbes associated with a newly discovered species of hydrothermal vent gastropod and therefore increase knowledge of ecosystem functioning in this largely unknown Antarctic hydrothermal vent system. We investigated the phylogenetic composition of bacteria associated with the gills and oesophageal gland of the ESR peltospirid gastropod, Gigantopelta chessoia by molecular cloning and terminal restriction fragment length polymorphism (T-RFLP). 16S rRNA gene clone libraries revealed host tissue-specific combinations of bacteria. The oesophageal gland contained one Gammaproteobacteria OTU whereas a more diverse community of Gamma, Epsilon and Deltaproteobacteria was isolated from the gills. T-RFLP analysis revealed that juvenile bacterial communities were more closely related to adult gill-associated bacterial communities than oesophageal gland bacteria. Oesophageal gland Gammaproteobacteria exhibited a higher sequence similarity with sulphur-oxidising bacteria isolated from cold seep sediments and with thioautotrophic endosymbionts than with bacteria found in the surrounding water column, suggesting that these endosymbionts were not acquired directly from the water column. Juvenile G. chessoia were located within the mantle cavity of adults and we speculate that Gammaproteobacterial endosymbionts in the oesophageal gland could be transmitted horizontally from adults to juveniles via the gills due to the close contact of juveniles with adults’ gills.
KeywordsSymbiont Hydrothermal vent Gastropod Antarctic Chemosynthesis Microbial diversity
The authors would like to thank the principal scientist of JC80 Prof. P. Tyler, the Master and crew of the RRS James Cook as well as the team of technicians of the ROV Isis. The Natural Environment Research Council (NERC) funded the study through the ChEsSO—Chemosynthetically driven ecosystems south of the Polar Front: biogeography and ecology consortium grant (grant number NE/D01249x/1).
- Cavanaugh CM, McKiness ZP, Newton ILG, Stewart FJ (2006) Marine chemosynthetic symbioses. In: Dworkin M et al (ed) The prokaryotes. A handbook on the biology of Bacteria. Vol 1 symbiotic associations, biotechnology and applied microbiology, 3rd Ed. Springer, New York, pp 475–507. doi: 10.1007/0-387-30741-9_18
- Chen C, Copley JT, Linse K, Rogers AD, Sigwart JD (2015a) The heart of a dragon: 3D anatomical reconstruction of the ‘scaly-foot gastropod’ (Mollusca: Gastropoda: Neomphalina) reveals its extraordinary circulatory system. Front Zool 12:13. doi: 10.1186/s12983-015-0105-1 CrossRefPubMedPubMedCentralGoogle Scholar
- Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0Google Scholar
- Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–175Google Scholar
- Nakagawa S, Shimamura S, Takaki Y, Suzuki Y, Murakami S, Watanabe T, Fujiyoshi S, Mino S, Sawabe T, Maeda T, Makita H, Nemoto S, Nishimura S, Watanabe H, Watsuji T, Takai K (2014) Allying with armored snails: the complete genome of gammaproteobacterial endosymbiont. ISME J 8:40–51. doi: 10.1038/ismej.2013.131 CrossRefPubMedGoogle Scholar
- Reid WDK, Sweeting CJ, Wigham BD, Zwirglmaier K, Hawkes JA, McGill RAR, Linse K, Polunin NVC (2013) Spatial differences in East Scotia Ridge hydrothermal vent food webs: influences of chemistry, microbiology and predation on trophodynamics. PLoS ONE 9(6):e65553. doi: 10.1371/journal.pone.006553 CrossRefGoogle Scholar
- Rogers AD, Tyler PA, Connelly DP, Copley JT, James R, Later RD, Linse K, Mills RA, Garabato AN, Pancost RD, Pearce DA, Polunin NV, German CR, Shank T, Boersch-Supan PH, Alker BJ, Aquilina A, Bennett SA, Clarke A, Dinley RJ, Graham AG, Green DR, Hawkes JA, Hepburn L, Hilario A, Huvenne VA, Marsh L, Ramirez-Llodra E, Reid WD, Roterman CN, Sweeting CJ, Thatje S, Zwirglmaier K (2012) The discovery of new deep-sea hydrothermal vent communities in the Southern Ocean and implications for biogeography. PLoS Biol 10(1):e1001234. doi: 10.1371/journal.pbio.1001234 CrossRefPubMedPubMedCentralGoogle Scholar
- Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75(23):7537–7541. doi: 10.1128/AEM.01541-09 CrossRefPubMedPubMedCentralGoogle Scholar
- Suzuki Y, Sasaki T, Susuki M, Nogi Y, Miwa T, Takai K, Nealson KH, Horikoshi K (2005) Novel chemoautotrophic endosymbiosis between a member of the Epsilonproteobacteria and the hydrothermal-vent gastropod Alviniconcha aff. hessleri (Gastropoda: Provannidae) from the Indian Ocean. Appl Environ Microbiol 71(9):5440–5450. doi: 10.1128/AEM.71.9.5440-5450.2005 CrossRefPubMedPubMedCentralGoogle Scholar
- Suzuki Y, Kojima S, Sasaki T, Suzuki M, Utsumi T, Watanabe H, Urakawa H, Tsuchida S, Nunoura T, Hirayama H, Takai K, Nealson KH, Horikoshi K (2006) Host-symbiont relationships in hydrothermal vent gastropods of the genus Alviniconcha from the Southwest Pacific. Appl Environ Microbiol 72(2):1388–1393. doi: 10.1128/AEM.72.2.1388-1393.2006 CrossRefPubMedPubMedCentralGoogle Scholar
- Zwirglmaier K, Reid W, Heywood J, Sweeting CJ, Wigham BD, Polunin NV, Hawkes JA, Connelly DP, Pearce D, Linse K (2015) Linking regional variation of epibiotic bacterial diversity and trophic ecology in a new species of Kiwaidae (Decapoda, Anomura) from East Scotia Ridge (Antarctica) hydrothermal vents. Microbiol Open 4(1):136–150. doi: 10.1002/mbo3.227 CrossRefGoogle Scholar